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Open Access Research article

The origin of modern frogs (Neobatrachia) was accompanied by acceleration in mitochondrial and nuclear substitution rates

Iker Irisarri1, Diego San Mauro2, Federico Abascal13, Annemarie Ohler4, Miguel Vences5 and Rafael Zardoya1*

Author affiliations

1 Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, 28006, Madrid, Spain

2 Department of Animal Biology, University of Barcelona, Av. Diagonal 643, 08028, Barcelona, Spain

3 Structural Computational Biology Group, Spanish National Cancer Research Center (CNIO), Melchor Fernández Almagro 3, 28029, Madrid, Spain

4 UMR 72205 OSEB, Département de Systématique et Evolution, Muséum National d’Histoire Naturelle, 25 rue Cuvier, CP 30, 75005, Paris, France

5 Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Mendelssohnstrasse 8, 38106, Braunschweig, Germany

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Citation and License

BMC Genomics 2012, 13:626  doi:10.1186/1471-2164-13-626

Published: 15 November 2012

Abstract

Background

Understanding the causes underlying heterogeneity of molecular evolutionary rates among lineages is a long-standing and central question in evolutionary biology. Although several earlier studies showed that modern frogs (Neobatrachia) experienced an acceleration of mitochondrial gene substitution rates compared to non-neobatrachian relatives, no further characterization of this phenomenon was attempted. To gain new insights on this topic, we sequenced the complete mitochondrial genomes and nine nuclear loci of one pelobatoid (Pelodytes punctatus) and five neobatrachians, Heleophryne regis (Heleophrynidae), Lechriodus melanopyga (Limnodynastidae), Calyptocephalella gayi (Calyptocephalellidae), Telmatobius bolivianus (Ceratophryidae), and Sooglossus thomasseti (Sooglossidae). These represent major clades not included in previous mitogenomic analyses, and most of them are remarkably species-poor compared to other neobatrachians.

Results

We reconstructed a fully resolved and robust phylogeny of extant frogs based on the new mitochondrial and nuclear sequence data, and dated major cladogenetic events. The reconstructed tree recovered Heleophryne as sister group to all other neobatrachians, the Australasian Lechriodus and the South American Calyptocephalella formed a clade that was the sister group to Nobleobatrachia, and the Seychellois Sooglossus was recovered as the sister group of Ranoides. We used relative-rate tests and direct comparison of branch lengths from mitochondrial and nuclear-based trees to demonstrate that both mitochondrial and nuclear evolutionary rates are significantly higher in all neobatrachians compared to their non-neobatrachian relatives, and that such rate acceleration started at the origin of Neobatrachia.

Conclusions

Through the analysis of the selection coefficient (ω) in different branches of the tree, we found compelling evidence of relaxation of purifying selection in neobatrachians, which could (at least in part) explain the observed higher mitochondrial and nuclear substitution rates in this clade. Our analyses allowed us to discard that changes in substitution rates could be correlated with increased mitochondrial genome rearrangement or diversification rates observed in different lineages of neobatrachians.

Keywords:
Substitution rate; Selection; Molecular dating; Mitochondrial genome; Mitogenomics; Anura; Neobatrachia; Evolution